The neuropeptide calcitonin gene-related peptide (CGRP) stimulates T cell migration into collagen matrices

Journal of Neuroimmunology

Volumn 196, Issue 1-2, 2008, Pages 60-66

  Talme, Toomas ^a   Liu, Zhiwen ^a   Sundqvist, Karl Gösta ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

CGRP; Extracellular matrix; Lymphocyte migration; Neuropeptides; T cell infiltration

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CD45RA ANTIGEN; CD45RO ANTIGEN; COLLAGEN; NEUROPEPTIDE;

ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CELL MIGRATION; HUMAN; MEMORY T LYMPHOCYTE; MIGRATION; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE;

ANALYSIS OF VARIANCE; ANTIGENS, CD; CALCITONIN GENE-RELATED PEPTIDE; CELL MOVEMENT; COLLAGEN TYPE I; DRUG INTERACTIONS; HUMANS; SOMATOSTATIN; T-LYMPHOCYTES;

EID: 44349134427     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2008.02.007     Document Type: Article

References (61)

1. Amara S.G., Arrizza J.L., Leff S.E., Swanson L.W., Evans R.M., and Rosenfeld M.G. Expression in brain of a messenger RNA encoding a novel neuropeptide homologous to calcitonin gene-related peptide. Science 229 (1985) 1094-1097
2. Asahina A., Hosoi J., Beissert S., Stratigos A., and Granstein R.D. Inhibition of the induction of delayed-type and contact hypersensitivity by calcitonin gene-related peptide. J. Immunol. 154 (1995) 3056-3061
3. Baggiolini M. Chemokines and leukocyte traffic. Nature 392 (1998) 565-568
4. Boudard F., and Bastide M. Inhibition of mouse T-cell proliferation by CGRP and VIP: effects of these neuropeptides on IL-2 production and cAMP synthesis. J. Neurosci. Res. 29 (1991) 29-41
5. Brain S.D., Williams T.J., Tippins J., Morris H.R., and MacIntyre I. Calcitonin gene-related peptide is a potent vasodilator. Nature 313 (1985) 54-56
6. Buckley C.D., Amft N., Bradfield P.F., Pilling D., Ross E., Arenzana-Seisdedos F., Amara A., Curnow S.J., Lord J.M., Scheel-Toellner D., and Salmon M. Persistent induction of the chemokine receptor CXCR4 by TGF-beta 1 on synovial T cells contributes to their accumulation within the rheumatoid synovium. J. Immunol. 165 (2000) 3423-3429
7. Bulloch K., Hausman J., Radojcic T., and Short S. Calcitonin gene-related peptide in the developing and aging thymus. An immunocytochemical study. Ann. N. Y. Acad. Sci. 621 (1991) 218-228
8. Bulloch K., McEwen B.S., Nordberg J., Diwa A., and Baird S. Selective regulation of T-cell development and function by calcitonin gene-related peptide in thymus and spleen. An example of differential regional regulation of immunity by the neuroendocrine system. Ann. N. Y. Acad. Sci. 1 (1998) 551-562
9. Butcher E.C., and Picker L.J. Lymphocyte homing and homeostasis. Science 272 (1996) 60-66
10. Crofford L.J., Sano H., Karalis K., Webster E.A., Friedman T.C., Chrousos G.P., and Wilder R.L. Local expression of corticotropin-releasing hormone in inflammatory arthritis. Ann. N.Y. Acad. Sci. (2000) 459-471
11. Dorsam G., Voice J., Kong Y., and Goetzl E.J. Vasoactive intestinal peptide mediation of development and functions of T lymphocytes. Ann. N. Y. Acad. Sci. 921 (2000) 79-91
12. Drissi H., Lasmolles F., Le Mellay V., Marie P.J., and Lieberherr M. Activation of phospholipase C-beta1 via Galphaq/11 during calcium mobilization by calcitonin gene-related peptide. J. Biol. Chem. 273 (1998) 20168-20174
13. Eskandari F., Webster J.I., and Sternberg E.M. Neural immune pathways and their connection to inflammatory diseases. Arthritis Res. Ther. 5 (2003) 251-265
14. Farber E., Lanigab S., and Boer J. The role of cutaneous sensory nerves in the maintenance of psoriasis. Int. J. Dermatol. 29 (1990) 418-420
15. Fernandez S., Knopf M.A., Shankar G., and McGillis J.P. Calcitonin gene-related peptide indirectly inhibits IL-7 responses in pre-B cells by induction of IL-6 and TNF-alpha in bone marrow. Cell. Immunol. 226 (2003) 67-77
16. Foster C.A., Mandak B., Kromer E., and Rot A. Calcitonin gene-related peptide is chemotactic for human T lymphocytes. Ann. N. Y. Acad. Sci. 657 (1992) 397-404
17. Giardino L., Giuliani A., Fernandez M., and Calzà L. Spinal motoneurone distress during experimental allergic encephalomyelitis. Neuropathol. Appl. Neurobiol. 30 (2004) 522-531
18. Goodman E.C., and Iversen L.L. Calcitonin gene-related peptide: novel neuropeptide. Life Sci. 38 (1986) 2169-2178
19. Grimsholm O., Rantapää-Dahlqvist S., and Forsgren S. Levels of gastrin-releasing peptide and substance P in synovial fluid and serum correlate with levels of cytokines in rheumatoid arthritis. Arthritis Res. Ther. 7 (2005) R416-R426
20. Hall A. G proteins and small GTPases: distant relatives keep in touch. Science 280 (1998) 2074-2075
21. Hosoi J., Murphy G.F., Egan C.L., Lerner E.A., Grabbe S., Asahina A., and Granstein R.D. Regulation of Langerhans cell function by nerves containing calcitonin gene-related peptide. Nature 363 (1993) 159-163
22. Ivanoff A., Ivanoff J., Hultenby K., and Sundqvist K.G. Infiltrative capacity of T leukemia cell lines: a distinct functional property coupled to expression of matrix metalloproteinase-9 (MMP-9) and tissue inhibitor of metalloproteinases-1 (TIMP-1). Clin. Exp. Metastasis 17 (1999) 695-711
23. Ivanoff J., Ivanoff A., and Sundqvist K.G. Defective chemokine production in T-leukemia cell lines and its possible functional role. Dev. Immunol. 7 (2000) 67-75
24. Ivanoff J., Talme T., and Sundqvist K.G. The role of chemokines and extracellular matrix components in the migration of T lymphocytes into three-dimensional substrata. Immunology 114 (2005) 53-62
25. Krueger G., and Ellis C.E. Psoriasis - recent advances in understanding its pathogenesis and treatment. J. Am. Acad. Dermatol. 53 (2005) S94-S100
26. Kruger L., Silverman J.D., Mantyh P.W., Sternini C., and Brecha N. Peripheral patterns of calcitonin-gene-related peptide general somatic sensory innervation: cutaneous and deep terminations. J. Comp. Neurol. 280 (1989) 291-302
27. Levite M., Cahalon L., Hershkoviz R., Steinman L., and Lider O. Neuropeptides, via specific receptors, regulate T cell adhesion to fibronectin. J. Immunol. 160 (1998) 993-1000
28. Lundy S.K., Sarkar S., Tesmer L.A., and Fox D.A. Cells of the synovium in rheumatoid arthritis. T lymphocytes. Arthritis Res. Ther. 9 (2007) 202
29. McGillis J.P., Humphreys S., and Reid S. Characterization of functional calcitonin gene-related peptide receptors on rat lymphocytes. J. Immunol. 147 (1991) 3482-3489
30. McGillis J.P., Rangnekar V., and Ciallella J.R. A role for calcitonin gene related peptide (CGRP) in the regulation of early B lymphocyte differentiation. Can. J. Physiol. Pharm. 73 (1995) 1057-1064
31. Nanki T., Hayashida K., El-Shi K., Girschick H.J., Yavuz S., Lipsky P.E., Gabalawy H.S., and Suson S. Stromal cell-derived factor-1-CXC chemokine receptor 4 interactions play a central role in CD4+ T cell accumulation in rheumatoid arthritis synovium. J. Immunol. 165 (2000) 6590-6598
32. Nickoloff B.J., Schroder J.M., von den Driesch P., Raychaudhuri S.P., Farber E.M., Boehncke W.H., Morhenn V.B., Rosenberg E.W., Schon M.P., and Holick M.F. Is psoriasis a T-cell disease?. Exp. Dermatol. 9 (2000) 359-375
33. Okajima K., and Harada N. Regulation of inflammatory responses by sensory neurons: molecular mechanism(s) and possible therapeutic applications. Curr. Med. Chem. 13 (2006) 2241-2251
34. Olesen J., Diener H.-C., Husstedt I.W., Goadsby P.J., Hall D., Meier U., Pollentier S., and Lesko L.M. Calcitonin gene-related peptide receptor antagonist BIBN 4096 BS for the acute treatment of migraine. N. Engl. J. Med. 350 (2004) 1104-1110
35. Panayi G.S., Lanchbury J.S., and Kingsley G.H. The importance of the T cell in initiating and maintaining the chronic synovitis of rheumatoid arthritis. Arthritis Rheum. 35 (1992) 729-735
36. Pablos J.L., Amara A., Bouloc A., Santiago B., Caruz A., Galindo M., Delaunay T., Virelizier J.L., and Arenzana-Seisdedos F. Stromal-cell derived factor is expressed by dendritic cells and endothelium in human skin. Am. J. Pathol. 155 (1999) 1577-1586
37. Payan D.G., and Goetzl E.J. Dual roles of substance P: modulator of immune and neuroendocrine functions. Ann. N. Y. Acad. Sci. 512 (1987) 465-475
38. Poyner D.R. Calcitonin gene-related peptide: multiple actions, multiple receptors. Pharmacol. Ther. 56 (1993) 23-51
39. Reubi J.C., Horisberger U., Kappeler A., and Laissue J.A. Localization of receptors for vasoactive intestinal peptide, somatostatin, and substance P in distinct compartments of human lymphoid organs. Blood 92 (1998) 191-197
40. Rosenfeld M.G., Emeson R.B., Yeakley J.M., Merillat N., Hedjran F., Lenz J., and Delsert C. Calcitonin gene-related peptide: a neuropeptide generated as a consequence of tissue-specific, developmentally regulated alternative RNA processing events. Ann. N. Y. Acad. Sci. 621 (1991) 1-17
41. Sakuta H., Inaba K., and Muramatsu S. Calcitonin gene-related peptide enhances apoptosis of thymocytes. J. Neuroimmunol. 67 (1996) 103-109
42. Sanchez-Madrid F., and del Pozo M.A. Leukocyte polarization in cell migration and immune interactions. EMBO J. 18 (1999) 501-511
43. Schor S.L., Allen T.D., and Winn B. Lymphocyte migration into three-dimensional collagen matrices: a quantitative study. J. Cell. Biol. 96 (1983) 1089-1096
44. Springer T.A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76 (1994) 301-314
45. Sternberg E.M. Neuroendocrine regulation of autoimmune/inflammatory disease. J. Endocrinol. 169 (2001) 429-435
46. Stevens-Felten S.Y., and Bellinger D.L. Noradrenergic and peptidergic innervation of lymphoid organs. Chem. Immunol. 69 (1997) 99-131
47. Sundqvist K.G., Hauzenberger D., Hultenby K., and Bergstrom S.E. T lymphocyte infiltration of two- and three-dimensional collagen substrata by an adhesive mechanism. Exp. Cell Res. 206 (1993) 100-110
48. Talme T., Ivanoff J., and Sundqvist K.G. Somatostatin is a specific inhibitor of SDF-1alpha-induced T cell infiltration. Clin. Exp. Immunol. 135 (2004) 434-439
49. Torii H., Hosoi J., Beissert S., Xu S., Fox F.E., Asahina A., Takashima A., Rook A.H., and Granstein R.D. Regulation of cytokine expression in macrophages and the Langerhans cell-like line XS52 by calcitonin gene-related peptide. J. Leukoc. Biol. 61 (1997) 216-223
50. Umeda Y., Takamiya M., Yoshizaki H., and Arisawa M. Inhibition of mitogen-stimulated T lymphocyte proliferation by calcitonin gene-related peptide. Biochem. Biophys. Res. Commun. 154 (1988) 227-235
51. Van Hagen P.M. Somatostatin receptor expression in clinical immunology. Metabolism 45 (1996) 86-87
52. Vissers W.H.P.M., Arndtz C.H.M., Muys L., VanErp P.E.J., DeJong E.M.G., and Van Der Kerkhof P.C.M. Memory effector (CD45RO+) and cytotoxic (CD8+) T cells appear early in the margin zone of spreading psoriasis lesions in contrast to cells expressing natural killer receptors, which appear late. Br. J. Dermatol. 150 (2004) 852-859
53. Voermans C., Anthony E.C., Mul E., van der Shoot E., and Hordijk P. SDF-1-induced actin polymerization and migration in human hematopoietic progenitor cells. Exp. Hermatol. 29 (2001) 1456-1464
54. Wang F., Millet I., Bottomly K., and Vignery A. Calcitonin gene-related peptide inhibits interleukin 2 production by murine T lymphocytes. J. Biol. Chem. 267 (1992) 21052-21057
55. Wang X., Fiscus R.R., Tang Z., Yang L., Wu J., Fan S., and Mathews H.L. CGRP in the serum of endotoxin-treated rats suppresses lymphoproliferation. Brain Behav. Immun. 8 (1994) 282-292
56. Wang H., Xing L., Li W., Hou L., Guo J., and Wang X. Production and secretion of calcitonin gene-related peptide from human lymphocytes. J. Neuroimmunol. 130 (2002) 155-162
57. Weihe E., Muller S., Fink T., and Zentel H.J. Tachykinins, calcitonin gene-related peptide and neuropeptide Y in nerves of the mammalian thymus: interactions with mast cells in autonomic and sensory neuroimmunomodulation?. Neurosci. Lett. 100 (1989) 77-82
58. Wilkinson P.C., Lackie J.M., Forrester J., and Dunn G.A. Chemokinetic accumulation of human neutrophils on immune complex-coated substrata: analysis at a boundary. J. Cell Biol. 99 (1984) 1761-1768
59. Wimalawansa S.J., Morris H.R., Etienne A., Blench I., Panico M., and MacIntyre I. Isolation, purification and characterization of beta-hCGRP from human spinal cord. Biochem. Biophys. Res. Commun. 167 (1990) 993-1000
60. Wimalawansa S.J. Calcitonin gene-related peptide and its receptors: molecular genetics, physiology, pathophysiology, and therapeutic potentials. Endocr. Rev. 17 (1996) 533-585
61. Wolf K., Müller R., Borgmann S., Bröcker E.-B., and Friedl P. Amoeboid shape change and contact guidance: T-lymphocyte crawling through fibrillar collagen is independent of matrix remodeling by MMPs and other proteases. Blood 102 (2003) 3262-3269